ISSN 1313 - 8820

Volume 8, Number 3
September 2016

2016
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ISSN 1313 - 8820 Volume 8, Number 3
September 2016

2016
AGRICULTURAL SCIENCE AND TECHNOLOGY, VOL. 8, No 3, pp 175 - 182, 2016
DOI: 10.15547/ast.2016.03.032

Review

Honey bees and their products as indicators of environmental pollution: A review

D. Salkova*, M. Panayotova-Pencheva

Department of Experimental Parasitology, Institute of Experimental Morphology, Pathology and Anthropology with Museum, Bulgarian Academy of
Sciences, Acad. G. Bonchev 25, 1113 Sofia, Bulgaria

(Manuscript received 18 January 2016; accepted for publication 8 August 2016)

Abstract. In the present work a literature review of the experiments that explore the use of honey bees and their products as bioindicator of environmental
pollution is presented. The greatest number of studies has been carried out on contaminations with heavy metals, followed by pesticides, radionuclides and
other substances. Pb, Cd and Zn have been the most looked for metals. Zn and Cd have been mainly deposited on the surface of the bee body while Ni, Cd, Pb
and Co have been released with the excrements most often. In all cases of pesticide implementation certain amounts of them have been always accumulated
in the bees and their products. According to the researchers, pollutants accumulate in the bees and their products at different extents. Heavy metals and
pesticides have been established in the bodies of honey bees in larger quantities in comparison to honey. Most of the authors reported that bee honey is a
suitable tool for monitoring pollution with heavy metals and pesticides but the opposite assertions have been also expressed. A suggestion for the presence of a
bio-barrier function of the bee organism against contaminators has been forwarded. It has been established that pollen is the most suitable indicator for
radioactive pollution. As a whole, the present review shows that bees and their products are suitable models for bio-monitoring of the environmental pollution of
different nature.

Keywords: honey bees, bee products, bioindicators, pollution, heavy metals, pesticides

Introduction It is well-known that at the time of active pasture bees gather

Environment is the factor together with the genetic background
of the human that influences to a great extent his health and quality
of life. In recent years as a result of the activity of man (harmful
emissions of burnt fuel, deforestation, the deposition of chemical,
radioactive and biological refuse, etc.) serious deviations from the
normal parameters recording the state of the environment have
been observed. The environmental changes on their part have their
effect on man directly or indirectly. For example, the contamination of
soil and water with heavy metals and chemicals leads to their
accumulation in the plants and animals inhabiting the polluted areas.
The human as an end consumer accumulates these pollutants, a
part of which (for example some heavy metals) are deposited in the
bones, teeth and stay there till the end of life having harmed his
health in the meantime.
The danger of negative changes in the environment makes
scientists look for novel, more efficient methods for monitoring the
environment for early detection of pollutants. Alongside with the
confirmed and widely used methods attempts are being made
recently for testing different biological species (plants, insects, fish
and other small animals) as bioindicators of changes (Chovanec et
al., 2003; Hijano et al., 2005; Nummelin et al., 2007; Sánchez-Chardi
et al., 2007). Bees in this respect, which are in constant contact with
the atmosphere, plants, waters and soils are the object of numerous
ecological studies aimed at establishing their role in the detection of
polluted areas. Great attention is also being paid to honey bee
products which also yield information about the state of the
surroundings inhabited by bees.
* e-mail: dsalkova@abv.bg
pollen and nectar in the radius of seven square kilometers (Tonelli et
al., 1990). Together with the nectar, propolis and pollen they
introduce a number of chemical and physical pollutants in the hive,
which pass into the honey and affect the production, health and life of
the bees.
The pollutants which exert influence on the bees and the bee
products can be of different nature. Such are, for example, the
contaminations which man willingly or unwillingly produces in his
everyday activities (burnt gases, heavy metals and metalloids,
radionuclides and other toxic emissions), pesticides used against
different harmful agents in agriculture, the veterinary-medical
preparations used in the struggle against viral, bacterial and
parasitoses in bees, etc. Bogdanov (2006) has divided these
pollutants into two main groups – those related to the activity of the
bee-keeper and the other caused by the state of the surroundings
from which the bees gather nectar and pollen. He has included in the
environmental group of pollutants the heavy metals, radioactive
isotopes, organic contaminators, pesticides (insecticides,
fungicides, herbicides and bactericides), pathogenic bacteria and
genetically modified organisms. In the group of pollutants driven into
the hive by the beekeeper. Bogdanov (2006) mainly relates the
acaricidic remedies used in the anti-parasite struggle as well as the
chemical remedies for fighting bacterial infections which also leave
traces in the honey, pollen, wax, propolis and royal jelly.
The bee acts as a detector of environmental pollution in two
ways, as it signals either via high mortality rates the presence of toxic
molecules, or via the residues in honey, pollen, and larvae the
presence of heavy metals, fungicides and herbicides that are
harmless to it. Bee monitoring also contributes to the ecological

175
impact statement by culminating in the charting of environmental
health maps, which include such data as mortality rates, apicide
number, type and risk-level of molecules detected, and so forth (Celli
and Maccagnani, 2003).
The aim of the present work is to provide a literature review of
the experiments that explore the use of honey bees and their
products as bioindicator of environmental pollution.
The results found are presented in a chronological order and
are assigned to three main groups of pollutants - heavy metals,
pesticides, radioactive and other agents.
Honey bees and their products as indicators of pollutions
with heavy metals
Heavy metals represent some of the most common and
dangerous pollutants of the environment. That is probably why a
large number of investigators have studied the role of bees and their
products as bioindicators for pollution with them.
Nineteen samples of honey taken from grocery shelves, near
zinc mines, adjacent to an industrial area, and near a major highway
have been subjected to spark source mass spectrometry to
determine the concentration of most of 47 elements in the honey
(Tong et al., 1975). Certain samples of honey produced by bees in
the vicinity of the New York State Thruway have contained elevated
levels of certain elements known to be emitted by traffic, such as Al,
Ba, Ca, Co, Mg, Ni, Pd, and Si, but the true source of these elements
has been uncertain. Honey which has been into contact with metal
containers in processing has contained the greatest amounts of Zn
and Sn.
The potential use of honey as an indicator in mineral
prospecting and environmental contamination studies has been
investigated by Jones (1987). Ag, Cd, Cu, and Pb levels content of
honey have been investigated in relation to that in the soils collected
from within the foraging area. For samples collected over two
seasons the following concentrations have been found Ag <0.1 to
6.5 ng. g−1 (d.w.); Cd <0.3 to 300 ng. g−1; Cu 35 to 6510 ng. g−1; Pb <2
to 200 ng. g−1. Considerable spatial and seasonal fluctuations have
been apparent. No correlations have been observed between honey
and soil concentrations for either Cu or Pb. It has been concluded
that the low concentrations of heavy metals in honey and their
inherent variability (due to differences in floral source, foraging
range, entrapment of atmospheric particulates on the flower, etc.)
detract from the reliable use of honey as a monitoring tool.
Leita et al. (1996) have carried out an experiment using 12
colonies of honey bees bred in hives located near an extraurban
crossroad. They have analyzed the Pb, Cd and Zn deposited on the
bee's surfaces and the heavy metal accumulation in the foragers,
dead bees, honey products and some environmental markers during
nine weeks of the experiment. Results have shown a large amount of
Zn and Cd on the bee's surface as a consequence of atmospheric
fallout, whereas according to authors Pb seems to be either water-
extractable and/or likely accumulated in the body of the insect. Dead
bees expelled from the hives have displayed a progressive
accumulation of all heavy metals during the experimental period.
Royal jelly and honey contained large amounts of heavy metals. The
obtained results have suggested that honey bee products may be
considered useful parameters to assess the presence of
environmental contaminants, whereas the measurements of heavy
metals in the dead bees may be considered a suitable tool also to
verify a possible dynamics of accumulation of pollutants.
The concentrations of three representative heavy metals (Cd,
176
Cr and Pb) have been measured by atomic absorption spectroscopy
in honeybees, honey, pollen, propolis, and wax (Conti and Botrè,
2001). Samples have been collected from five different sampling
points: four from areas surrounding the city of Rome, and the fifth in
the city center which receives intensive traffic. All apiaries employed
for the study have been specifically constructed without any metal
part in order to avoid the risk of contamination of the assayed
materials. Experimental data have revealed, in general, statistically
significant differences between the background levels of heavy
metals recorded from the reference sites and the levels measured in
the site located in the center of the city of Rome. According to authors
the results have indicated that honeybees and, to a lesser extent,
some of their products (pollen, propolis, wax, but not honey), can be
considered representative bioindicators of environmental pollution.
Concentrations of 137Cs in various honey types during the 1990s
in Croatia were recorded by Barišic´ et al. (2002). The research has
also documented the levels of 137Cs, 40K, Ca, Fe, Rb, Sr, Cu, Zn, Pb,
Ni, Mn, and Cr in soils, coniferous tree branches and honey, and has
compared the transfer from soil into nectar honey, mixtures of nectar
and honeydew honey, and honeydew honey in fir and spruce forests
in Croatia. For all of the elemental concentrations investigated, no
significant differences have been found between honeydew honey
and mixed honey, regardless of the soil type where the honey has
been collected from. Elemental transfer factors from soils into nectar
honey have been significantly lower than those for honeydew honey.
The research about chemical contamination of honey
harvested from beehives situated in Copsa Mica (Sibiu region),
famous for the ecological unbalances induced by the non-ferrous
metal industry has been carried out by Bratu and Georgescu (2005).
The amount of Pb, Cd and Zn contained in the honey samples has
been determined using an atomic absorption spectrometer.
Amounts of heavy metals above the admitted limit have been
discovered.
Thirteen metal elements have been determined in 40 honey
samples from Galicia with different environmental origins: rural,
urban, and industrial areas (Rodríguez García et al., 2006). The data
set of the honey metallic profiles has been studied with a double
purpose: first, to make a preliminary evaluation of honey as an
environmental indicator in Galicia with the aim of monitoring
pollution and, second, to compare the different capabilities of
diverse pattern recognition prediction procedures for modeling the
environmental surrounding of the hive. A certain level of similarity for
urban and industrial samples has been obtained using principal
component analysis and cluster analysis, whereas significant
differences for urban and industrial honeys have been found in
relation to rural honey samples. According to authors the metal
profiles of honey seem to provide sufficient information to enable
categorization criteria for classifying samples according to their
environmental surrounding. Thus, honey could be a potential
pollution indicator for the Galician area.
Nine heavy metals, Co, Cd, Cr, Cu, Fe, Mn, Ni, Pb, and Zn, have
been determined in a total of 192 samples (96 soil, 48 flower, and 48
honey samples), which have been collected from polluted areas
(Edfu and Kom Omb cities) and unpolluted areas (Esna and Aneeba
cities) at Aswan district, Egypt (Rashed et al., 2009). Metal
concentrations have been measured using an atomic absorption
spectrophotometer. The results have revealed that honey in polluted
areas showed higher concentrations of Cu, Pb, Fe, and Zn than
honey from unpolluted areas. This has been related to the pollution
input from industrial activities in polluted areas. A study of metal
concentrations in flowers has revealed that flowers contained the
highest levels of the studied metals than those in honey.
Concentration factors of heavy metal for honey/flower in polluted
areas seem to be higher than in that of the unpolluted ones. Element
concentrations in honey have been within the safety baseline levels
for human consumption. The results have suggested that honey
may be useful as an environmental indicator for assessing the
presence of environmental pollution with heavy metals.
Zhelyazkova et al. (2010) have carried out a comparative
analysis of the content of some heavy metals and metalloids (Cu, Zn,
Pb, Cd, Ni, Co, Mn, Fe) in the body of bees, fecal mass, bee products
(honey, pollen, wax) and sunflower flowers in areas with different
degree of anthropogenic impact. The study has included two
settlements in Stara Zagora region (Bulgaria): the town of Gurkovo –
an area with low level of anthropogenic impact; the village of Bratya
Kunchevi – an area with established anthropogenic impact (working
stone quarry on the territory of the village). Accumulation of the
studied heavy metals and metalloids in the bee fecal mass has been
observed and high level of accumulation in excrements has been
exhibited by Pb (1:2,3 - 1:4,0), Cd (1:1,6 - 1:1,9), Ni (1:4,2 - 1:4,3), Co
(1:1,6 -1:2,0). The bio-barrier function of the bee organism has been
proved as a result of which heavy and toxic metals such as Pb and
Cd have been efficiently excreted by the organism through the fecal
mass. It has been established that Fe content has been of higher
values in the bee body, pollen and wax in the station village of Bratya
Kunchevi (compared to the samples in the town of Gurkovo).
According to authors a possible reason for the reported high quantity
of iron in the analyzed samples of the village of Bratya Kunchevi
could be the working stone quarry on the territory of the village
operating a deposition of andesite tuffs (calcium-magnesium-iron
silicates). Unsatisfactory indicator characteristics of bee honey for
environmental quality have been established in areas with different
degree of anthropogenic impact compared to bee organism and
pollen.
Sadeghi et al. (2012) have determined the levels of some
elements (Hg, Ba, Ca, Fe, Mn, Li, As, Na and K) in the bodies of
bees. Honeybee samples have been randomly collected from
apiaries located in four counties of the province of Kurdistan. The
obtained data have shown that K has had the highest concentration,
followed by Na, Ca, Hg, Ba, Fe, Mn, Li and As. Three mineral groups
have been differentiated: elements very abundant, in a medium
concentration, and trace ones. The first group consisted of K and Na,
with a range from 41.857 to 47.871, and 12.653 to 16.183 ppm,
respectively. The second mineral group has been composed of Ca,
Hg, Ba, and Fe, where Ca was the most abundant element (with a
range of 9.077 to 10.058 ppm), followed by Hg (1.12-4.786 ppm), Ba
(2.881-3.481 ppm), and Fe (1.050-1.727 ppm). The third mineral
group has been composed of Mn, Li and As in range from 0.262 to
0.399, from 0.043 to 0.101, and from 0.017 to 0.068 ppm,
respectively.
Roman and Popiela-Pleban (2012) have determined the extent
of bioaccumulation of toxic elements Zn, Cu, Pb, As and Cd in
propolis collected in Opole area. The sequence of accumulation
level of the studied elements in propolis has been as follows:
Zn>Cu>Pb>As>Cd. An average concentration of Zn, Cu, Pb, As and
Cd has amounted to 56.28, 7.12, 6.91, 0.745, 0.218 mg.kg-1,
respectively. Only the Cu average content in propolis has been
within acceptable standards, whereas the mean contents of the
other elements have greatly exceeded these standards.
Zhelyazkova (2012) has tested honeybees as bioindicators for
environmental status in the region of Sarnena Sredna gora, county
of Stara Zagora, Bulgaria. The study comprised six villages, located
close to the military range of Zmeyovo. In each village bee samples
were taken and samples of whole bees and fecal mass were
prepared. The content of Cu, Zn, Pb, Cd, Co, Ni, Mn and Fe were
traced in the bee body and in excrements. The analysis was carried
out through atomic absorption spectrometry according to ISO
11047. Maximum or relatively high values for content of the studied
heavy metals and metalloids in the body and fecal mass of bees
were found, which has made it possible to comment a possible
anthropogenic effect in the area of Sarnena Sredna gora, Zmeyovo
military range. Higher content of the studied heavy metals and
metalloids in excrements compared to the body of bees was found,
which has accounted for the bio-barrier function of the bee organism.
The elements Ni, Cd, Co and Pb have been accumulated at the
highest degree in the bee fecal mass. The author assumes that
honeybees respond to changes in their environment and in
particular to increased quantities of heavy metals in soil, air, plants
and that makes them a reliable indicator and allows their use in bio-
monitoring of the environment.
Honey samples have been collected in different places of
Slovakia aiming to determine the concentration of heavy metals in
honey (Lazor et al., 2012). The results obtained in site Prievidza
during the 2006 – 2008 period were as follows: 0.0599 mg.kg-1 As,
0.0948 mg.kg-1 Cd, 0.0747 mg.kg-1 Cr, 0.0394 mg.kg-1 Hg and 0.1252
mg.kg-1 Pb and in site Šaľa: 0.0862 mg.kg-1 As, 0.0942 mg.kg-1 Cd,
0.0736 mg.kg-1 Cr, 0.0341 mg.kg-1 Hg and 0.1626 mg.kg-1 Pb. The
authors suggested that honey could be used to detect contaminating
agents in the environment.
Dima et al. (2012) evaluated the use of pollen as bioindicator of
environmental pollution. The content of Fe, Mn, and Zn from pollen
samples uniformly distributed in Dambovita County has been
determined using the Energy Dispersive X-Ray Fluorescence
Spectrometry. The samples have been collected from private farms,
kipped in industrial-urban and non industrial rural areas. The authors
have found differences between the two kinds of samples and have
concluded that pollen can be used for bio-monitoring the
environment for Fe, Mn, and Zn.
Total arsenic (t-As) and inorganic As (i-As) concentrations were
determined by Bastías et al. (2013) in 227 samples of honey
harvested during the years 2007, 2008, and 2009 in the areas of San
Pedro de Atacama, Atacama, Chiloé, and Futaleufú, with the last
town located 156 km from the Chaitén Volcano (latest eruption in
2008). These analyses have been conducted using an atomic
absorption spectrophotometer coupled with a hydride generator. In
the honey samples the concentrations of t-As ranged from 2.2 to
171.9 μg.kg-1, and the i-As concentrations - from none detected (ND)
to 24.6 μg.kg-1, with the area of San Pedro de Atacama having the
highest As concentrations. The samples of honey from Futaleufú
showed higher As concentrations after the eruption of the Chaitén
Volcano in 2008. According to authors the study demonstrates that
As pollution in honey may originate from both natural and
anthropogenic sources. The results have indicated that it is
appropriate to use honey as a bioindicator of environmental
pollution.
Ruschioni et al. (2013) have carried out bio-monitoring with
honeybees aiming to assess the presence of heavy metals (Cd, Cr,
Ni, Pb) in all of the ten nature reserves of the Marche Region
(central–eastern Italy). The study was performed during the spring
and summer seasons when honeybees were active, over 3 years
(2008–2010). Twenty-two colonies of honeybees bred in hives were
used. Samples of live and dead honeybees and of honey were
collected from 11 sampling stations from May to October in each
year. No pesticide pollution was found. Significant differences in
177
heavy metal concentrations were found among years, months and
sites, and in particular situations. The analysis has revealed that
high heavy-metal concentrations have occurred exclusively in live
honeybees. The most detected heavy metal was Cr, which
exceeded the threshold more often than for the other elements,
followed by Cd and Pb; Ni has never exceeded the threshold.
Formicki et al. (2013) have studied concentrations of Cd, Ni, Pb,
Fe, Mg, and Zn in multi-floral honey, propolis, bee pollen, and wax
coming from apiaries situated in different locations in Malopolska
Voivodeship in Poland. The authors have established that honey
contained the lowest concentrations of all the tested metals, with Cd
and Pb concentrations well below allowable levels. Other products
have showed much higher concentration of Cd and Pb. Propolis and
pollen from certain areas were significantly contaminated with Pb.
High metal contents occurred in beeswax. Positive correlations
between metals occurred in wax: Cd vs. Ni, Cd vs. Fe, Ni vs. Fe, Ni
vs. Mg, Pb vs. Fe, and Fe vs. Mg. Metal contents in honey did not
correlate with metal contents in other tested products. Correlations
between Fe concentrations in honey and wax and between Mg in
bee pollen and propolis were exceptional. The authors consider that
honeybee products may be useful in monitoring environmental
contamination by metals.
Steen et al. (2015) have explored whether honeybees could be
used as a reliable alternative to the standard mechanical devices for
monitoring air quality, in particular with respect to the concentration
of the heavy metals Cd, Pb and V. They have tested whether the
concentrations of these metals in adult honeybees and in ambient air
have been positively correlated, and whether differences in
concentration between locations have been similar for bees and air.
Measurements have been conducted over two-month period at
three distinct locations in the Netherlands with each three replicate
honeybee colonies placed next to mechanical monitoring devices
and they have shown that a significant positive relationship between
the concentrations in bees and in air could only be established for V.
Also, only in the case of V, the differences between the three
locations in mean concentration have been similar for bees and air.
Both outcomes have been probably due to the relatively large range
over which the concentrations of V varied, both in bees and in air, as
compared to Cd and Pb. However, for V, as well as for Cd and Pb, the
concentrations in ambient air have been about two orders of
magnitude below the established air quality standards. Therefore,
the authors have concluded that in the Netherlands, both variation
and levels of the atmospheric concentrations of these metals are too
low to establish a relationship between the concentration in bees
and in air that is useful to present honeybees as an alternative to
mechanical devices in monitoring air pollution. However, they
consider that in countries with larger variation and higher levels of
the atmospheric concentrations of these metals, further exploration
of the potential of honeybees in bio-monitoring air pollution may be
worthwhile.
A study by Aghamirlou et al. (2015) has indicated that all types
of honey contain metals and the metal concentrations vary among
different regions because of some variables. Findings have showed
that Zn and As have had the maximum and minimum concentrations,
respectively. The authors consider that some geological and
geochemical parameters may affect the honey chemistry. They also
have pointed that the proximity to the industries, having different
types of soil, using various fertilizers, and the diversity in the practice
of growing plants probably led to some differences between regions.
In their study, it has been difficult to compare the obtained results
with related standards, because some standards were based on
daily or weekly intake of metals, while there was no data about daily
178
consumption of honey by people. Finally, according to literature,
authors have mentioned some recommendations, namely: limiting
the consumption of hazardous fertilizers, monitoring the soil in
agricultural regions, considering the distance of agricultural lands
and flower gardens with industries, controlling the quality of food
products, providing some accurate standard limits for hazardous
compounds in the foods, and monitoring the water that is used for
agriculture and floriculture.
Honey bees and their products as indicators of pollution
with pesticides
According to some authors the utilization of different types of
pesticides in agriculture can be established by detecting traces of
them in bees and bee products.
According to Porrini et al. (2003) in many cases, pollution
caused by abuse or by erroneous application of pesticides could not
be proven without the help of honey bees. This group of authors has
carried out a monitoring of pesticides with honey bees. This work has
been applied in some areas surrounding Bologna. Each monitoring
station consisted of two beehives equipped with collection cages for
dead bees. Once a week, families were checked and the number of
dead bees was recorded. When the mortality rate exceeded the
critical threshold (250 bees/week/station), laboratory analysis was
carried out. The authors indicated periods of major bee poisoning
risk, and identified the most frequently used pesticides (also those
that are prohibited) and the crops treated. These studies with honey
bees have revealed the type of plant protection management
applied to the area under investigation and allowed to prove the
application of molecules not permitted under certain circumstances
or even forbidden.
Samples of honeybees from 14 beehive monitoring stations
located in 3 townships in the province of Bologna were aiming to
evaluate the concentration of 32 organophosphorus pesticides and
5 carbamates (Ghini et al., 2004). The most contaminated samples
were from Granarolo Emilia where cereals (wheat, sorghum, and
corn), sugar beets, and potatoes were the main agriculture products.
Thirty-five pesticides were detected, with organophosphorus being
the most abundant one. Malathion was detected in 58% of the
samples (mean level 0.360 mg/kg) followed by fenithrothion in 53%
of the samples (mean level 0.544 mg/kg) and pirimiphos methyl in
48% of the samples (mean level 0.006 mg/kg). Temporal trends
have showed that the maximum detection frequency occurred in late
spring and was associated with the use of treatment products and
less rainfall. The results have demonstrated the feasibility of using
honeybees for assessing pesticide exposure in agriculture settings.
A field survey has been performed on French apiaries to
monitor weakness of honey bee colonies (Chauzat et al., 2006). Five
colonies have been randomly selected in each apiary, leading to a
total of 125 studied honey bee colonies. For 3 years colonies were
visited four times per year: after winter, before summer, during
summer, and before winter. Pollen loads from traps were collected at
each visit. Multiresidue analyses have been performed in pollen to
search residues of 36 different molecules. Specific analyses have
been conducted to search fipronil and metabolites and also
imidacloprid and metabolites. Residues of 19 searched compounds
have been found in samples. Contamination by pesticides ranged
from 50 to 0%. Coumaphos and tau-fluvalinate residues have been
the most concentrated of all residues (mean concentrations - 925.0
and 487.2 μg/kg, respectively). Fipronil and metabolite contents
have been superior to the limit of detection in 16 samples. Residues
of fipronil have been found in 10 samples. Nine samples contained
the sulfone compound, and three samples contained the desulfinyl
compound. Residues of imidacloprid and 6-chloronicotinic acid have
been found in 69% of samples. Imidacloprid contents has been
quantified in 11 samples with values ranging from 1.1 to 5.7 μg/kg. 6-
Chloronicotinic acid content has been superior to the limit of
quantification in 28 samples with values ranging from 0.6 to 9.3
μg/kg.
The pollution of six agricultural areas of Greece by insecticides
used in crop protection has been investigated utilizing bee honey
produced in those areas as bioindicator (Balayiannis and
Balayiannis, 2008). Honey samples collected randomly from
apiaries located in those areas have been analyzed for pesticide
residues with a multi-analytical method, able to determine
simultaneously up to 10 organophosphorous insecticides from the
same honey extract. Findings concerning the acaricide coumaphos
have also been included, even though it is not used in crop
protection. The above areas are planted to a large extent with citrus
trees or cotton or sunflower crops which are good forages for
honeybees. The main pests of those crops are insects; hence,
insecticides are used on a large scale for crop protection. The most
contaminated samples originated from citrus groves; 16 out of 19
had pesticide residues: 4 samples had chlorfenvinphos (21.05%),
10 had chlorpyrifos (52.63%) and 2 - phorate (10.53%). Out of 17
samples from cotton fields, residues have been found in 8, phorate in
6 (35.29%), chlorfenvinphos in 1 (5.88%), and chlorpyrifos in 1
(5.88%). Out of nine samples from fields of sunflower, four had
phorate residues (44.44%). In brief, from the 50 analyzed samples,
Table 1. Comparative data about the use of honey bees and their products as indicator of environmental pollution with
heavy metals
Investigated products and origin Pollutants
Honey taken from grocery shelves, near zinc 47 different
mines, adjacent to an industrial area, and elements
near a major highway.
Honey has been investigated in relation to Ag, Cd, Cu, Pb
that in the soils collected from within the
foraging area of the bees.
12 colonies of honey bees bred in hives Pb, Cd, Zn
located near an extraurban crossroad: the
bees' surfaces, foragers, dead bees, honey
products.
Honey bees, honey, pollen, propolis, and Cd, Cr, Pb
wax have been collected from areas
surrounding the city of Rome, and the city
center which receives intensive traffic.
137
Nectar-honey, mixed honey, honeydew Cs, 40K, Ca, Fe, Elemental transfer factors from soils into
honey, soils, coniferous tree branches. Rb, Sr, Cu, Zn, Pb, nectar honey have been significantly lower
Ni, Mn, Cr
residues of chlorfenvinphos have been detected in 5 samples (10%),
residues of chlorpyrifos in 11 samples (22%), and residues of
phorate in 12 samples (24%). Their levels ranged between 0.70 and
0.89 μg/kg. Coumaphos residues ranged from 0.10 up to 4.80 μg/kg
and have been derived exclusively from beehives treated with
Perizin (the commercial formulation of coumaphos) for Varroa
control. This study has indicated that in agricultural areas with
developed apiculture useful information about the occurrence and
the distribution of pesticide residues due to crop protection
treatments can be derived from the analysis of randomly collected
honey samples used as bioindicators. It has also shown that, very
often, the chemicals used by apiculturists inside the hives in order to
control disease are the main pollutants of the produced honey.
Honey bees and their products as indicators of pollutions
with radioactive and other agents
Samples of honey, pollen and honey bees have been collected
in some regions of Italy after the accident in Chernobyl Nuclear
Power Plant (1986) and subjected to gamma spectrometry in order
to assess their possible use as markers of the radioactive
environmental contamination (Tonelli et al., 1990). Pollen has
resulted in the best indicator, since it reflects exactly the air
contamination and according to authors it is suitable for obtaining a
map of fallout. The authors have determined that bees can be used
for the purpose too, even if their collection is more difficult, whereas
honey has given only an indication.
Results / Conclusions Authors
The samples have contained elevated levels Tong et al. (1975)
of certain elements known to be emitted by
traffic, such as Al, Ba, Ca, Cu, Mg, Ni, Pd, and
Si. Honey which has been in contact with
metal containers in processing contained the
greatest amounts of Zn and Sn.
Considerable spatial and seasonal fluctuations Jones et al. (1987)
in the results have been apparent. No
correlations have been observed between
honey and soil concentrations for either Cu or
Pb.
Dead bees expelled from the hives have Leita et al. (1996)
displayed a progressive accumulation of all
heavy metals. Royal jelly and honey contained
large amounts of heavy metals. Zn and Cd
accumulate mainly on the bee's surface and
Pb - in the body.
Honey bees and, to a lesser extent, some of Conti and Botrè
their products (pollen, propolis, wax, but not (2001)
honey), can be considered representative bio-
indicators of environmental pollution.
Barišic´ et al.
(2002)
than those for honeydew honey. For all of the
elemental concentrations no significant
differences have been found between
honeydew honey and mixed honey, regardless
of the soil.
179
Honey from beehives situated in region
ecologically unbalanced by non-ferrous
metal industry.
Honey from different environmental origins:
rural, urban, and industrial areas.
Samples of soil, flower, and honey from
polluted areas and unpolluted areas.
Bodies of bees, fecal mass, bee products
(honey, pollen, wax) and sunflower flowers
from areas with different degree of
anthropogenic impact.
Bodies of bees from different regions.
Propolis.
Bee bodies and bee excrements from
villages located close to a military range.
Honey from different regions.
Pollen samples collected from private farms,
kipped in industrial-urban and non industrial
rural areas.
Honey from different regions, including ones
situated near the Chaitén Volcano, latest
erupted in 2008.
Samples of live and dead honey bees and
honey during the spring and summer
seasons over 3 years' period.
Honey, propolis, bee pollen, and wax from
different regions.
Concentrations of some metals have been
tested in honey bees and air.
Honey from different types and regions.
180
Pb, Cd, Zn Amounts of heavy metals above the admitted Bratu and
limit have been discovered. Georgescu (2005)
13 metal elements Honey could be a potential pollution indicator. Rodríguez García
et al. (2006)
Co, Cd, Cr, Cu, Fe, Concentration factors of heavy metal for Rashed et al.
Mn, Ni, Pb, Zn honey/flower in polluted areas seem to be (2009)
higher than in that of the unpolluted ones.
Cu, Zn, Pb, Cd, Ni, The biobarrier function of the bee organism Zhelyazkova et al.
Co, Mn, Fe has been proved as a result of which heavy (2010)
and toxic metals such as Pb and Cd have
been efficiently excreted by the organism
through the fecal mass.
Hg, Ba, Ca, Fe, Three minerals groups have been Sadeghi et al.
Mn, Li, As, Na, K differentiated: elements very abundant, in a (2012)
medium concentration, and trace ones.
Bee honey is a suitable bioindicator.
Zn, Cu, Pb, As, Cd Only the copper average content in propolis Roman and
has been within acceptable standards, Popiela-Pleban
whereas the mean contents of other elements (2012)
have greatly exceeded these standards.
Cu, Zn, Pb, Cd, Higher content of the studied heavy metals Zhelyazova (2012)
Co, Ni, Mn, Fe and metalloids in excrements compared to the
body of bees has been found, which has
accounted for the bio-barrier function of the
bee organism.
Heavy metals The authors suggested that honey could be Lazor et al. (2012)
used to detect contaminating agents in the
environment.
Fe, Mn, Zn Pollen can be used for bio-monitoring of Dima et al. (2012)
environment.
Total As, inorganic Pollution with As in honey may originate from Bastías et al.
As both natural and anthropogenic sources. It is (2013)
appropriate to use honey as a bioindicator of
environmental pollution.
Cd, Cr, Ni, Pb Significant differences in heavy metal Ruschioni et al.
concentrations have been found among years, (2013)
months and sites, and in particular situations.
The analysis has revealed that high heavy-
metal concentrations have occurred
exclusively in live honey bees.
Cd, Ni, Pb, Fe, Mg, Metal contents in honey have not been Formicki et al.
Zn correlated with metal contents in other tested (2013)
products. High metal contents have occurred
in beeswax. Honey contained the lowest
concentrations of all tested metals.
Cd, Pb, V In countries with larger variation and higher Steen et al. (2015)
levels of the atmospheric concentrations of
these metals, further exploration of the
potential of honey bees in bio-monitoring of air
pollution may be worthwhile.
Zn, As All types of honey contain metals and the Aghamirlou et al.
metal concentrations vary among different (2015)
regions because of some geological,
geochemical and anthropological factors.
Table 2. Comparative data about the use of honey bees and their products as indicator of environmental pollution with
pesticides and other agents.

Investigated products
and origin Pollutants Results / Conclusions Authors

Dead honey bees Pesticides The honey bees can be used for detection of pollution with pesticides. Porrini et al. (2003)
Honey bees Organophos- The results have demonstrated the feasibility of using honey bees for Ghini et al. (2004)
phorus pesticides, assessing pesticide exposure in agriculture settings.
carbamates
Pollen 36 different Contamination by pesticides ranged from 50 to 0%. Coumaphos and Chauzat et al. (2006)
molecules of tau-fluvalinate residues have been the most concentrated of all residues.
pesticides Bee pollen is suitable for detection of residues of pesticides.
Honey Insecticides In agricultural areas with developed apiculture, useful information about Balayiannis and
the occurrence and the distribution of pesticide residues due to crop Balayiannis (2008)
protection treatments can be derived from the analysis of randomly
collected honey samples, used as bioindicators. Very often, the
chemicals used by apiculturists inside the hives in order to control
diseases are the main pollutants of the produced honey.
Honey, pollen and Radioactive Pollen is the best indicator for radioactive contamination. Tonelli et al. (1990)
honey bees have contamination
were collected in Italy
after the Chernobyl
accident.
Honey SO2 The amount of sulphate determined in honey correlated with total yearly Ponikvar et al. (2005)
emissions of SO2 observed by an electronic monitoring.

A bee monitoring net consisting of 32 apiaries and covering an
area of about 700 km2 has been configured surrounding the Šoštanj
coal-fired power plant (Ponikvar et al., 2005). The results of
investigations have revealed that the amount of sulphate
determined in honey from this area correlated with total yearly
emissions of SO2 observed by an electronic monitoring. When
exhaust gases at the power plant were purified, a corresponding
decrease in the amounts of sulphate in honey has been observed.
According to authors, the proposed bee monitoring net is an
example of using bio-monitoring for tracing environmental pollution,
which could be also applied to estimate the impact of NOx gases or
to trace other pollutants.
The extraction from the above mentioned studies is shown in
Table 1 and Table 2.
Conclusion
The summing-up and analysis of the presented literature data
give us grounds for drawing the following conclusions:
The greatest number of the studies on bees and their products
as bioindicators of the environmental pollutions have been carried
out on contaminations with heavy metals followed by that with
pesticides, radionuclides and other substances.
Of the metals, Pb, Cd and Zn are the ones most looked for and
Fe, Mn, Ni, Cr, Cu, As and others more rarely. It has been established
that Zn and Cd are mainly deposited on the surface of the bee body
while Ni, Cd, Pb and Co are released with the excrements most
often.
It has become clear from the literature references made that in
all cases of pesticide implementation certain amounts of them are
always accumulated in bees and their products.
Honey is most often tested for pollutants followed by the bee
body, pollen, wax, propolis and faecal masses of bees. Studies on
royal jelly, nectar honey and honeydew are in single numbers.
As a whole, the authors quoted in the present study think that
bees and their products are suitable bioindicators of environmental
pollutions. According to the studies of those of them who have
compared the role of different bee products as bioindicators we have
arrived to the conclusion that pollutants accumulate in bees and their
products at different extent. Higher content of heavy metals and
metalloids was found in excrements of bees compared to the body,
which accounts for the bio-barrier function of the bee organism.
Honeybees and, to a lesser extent, some of their products (pollen,
propolis, wax), can be considered representative bioindicators of
environmental pollution. Other authors, however, have assumed
that bee honey is not among the appropriate bioindicators as
compared to pollen and bees have only yielded tips for their possible
use as bioindicator.
Generally it can be stated that the present literature review
undisputedly shows that bees and their products are a suitable
model for bio-monitoring of environmental pollution of various kind
which renders them a promising subject for future studies in this
field.
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AGRICULTURAL SCIENCE AND TECHNOLOGY, VOL. 8, No 3, 2016

CONTENTS 1/2

Review

Honey bees and their products as indicators of environmental pollution: A review 175
D. Salkova, M. Panayotova-Pencheva

Genetics and Breeding

Characterization of the Bulgarian sunflower hybrid Valin 183

G. Georgiev

Evaluation of the combining ability of mutant maize lines 189

V. Valkova, N. Petrovska

Evaluation of small size fruit peppers Capsicum annuum spp. microcarpum with cluster and factor 193
analysis
V. Kuneva, M. Nikolova

Sensitivity of promising cherry hybrids and new cultivars to economically important fungal diseases 197
K. Vasileva, S. Malchev, A. Zhivondov

Nutrition and Physiology

Lysozyme levels in haemolymph of worker bees (Apis mellifera L.) from bee colonies with different 201
degree of expression of hygienic behaviour
S. Lazarov, I. Zhelyazkova, D. Salkova, R. Shumkova, S. Takova

Production Systems

Study on energy flows of renewable sources for producing hot water on dairy farms 205
R. Georgiev, K. Peychev, D. Georgiev, R. Slavov, S. Apostolov, J. Ellingsen, J. Tønnesen

Loose smut of barley grown in three types of farming 209

T. Nedelcheva, V. Maneva

Efficacy and timing of some new products against pear psylla (Cacopsylla pyri L.) (Hemiptera: 213
Psyllidae): I. Spirotetramat
V. Arnaudov

Influence of year`s characteristics and the different fertilization levels on the structural elements of 217
wheat yield
V. Kuneva, R. Bazitov, A. Stoyanova
AGRICULTURAL SCIENCE AND TECHNOLOGY, VOL. 8, No 3, 2016

CONTENTS 2/2

Grain combines productivity according to various unloading methods – in the field and at the edge 221
of the field
N. Delchev, K. Trendafilov, G. Tihanov, Y. Stoyanov

Agriculture and Environment

Effect of some herbicides on weeds and vines in mother plantation of Cabernet sauvignon 227
N. Prodanova – Marinova

Influence of foliar herbicides treatment on malting barley (Hordeum vulgare L.) productivity of 232
Emon, Vanessa and Vicky varieties
D. Atanasova, V. Maneva

Selectivity and stability of herbicides and herbicide combinations for the grain yield of maize (Zea 237
Mays L.)
G. Delchev, T. Barakova

Effect of some soil herbicides on vegetative habits of almond trees of 'Nonpareil' cultivar grown in 242
a second-year nursery field
Z. Rankova, M. Tityanov

Phytosanitary conditions of the organic field and boundary 245

D. Atanasova, V. Maneva, N. Grozeva

Product Quality and Safety

Quality traits of eggs from autosexing Easter eggers 249

H. Lukanov, A. Genchev, A. Pavlov, I. Penchev

Amino acid composition of lamb meat from the North East Bulgarian fine fleece breed and its 256
crossbreds from internal breeding
R. Slavov, G. Mihaylova, St. Ribarski, D. Panayotov, D. Pamukova, D. Dragnev

Some results of evaluation of new-introduced apricot cultivars under conditions of Plovdiv region 262
V. Bozhkova, M. Nesheva
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Peters), vol. 22, 143-165, Pergamon
Press. Oxford, UK.
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The Editorial Board of the Journal is not
responsible for incorrect quotes of
reference sources and the relevant
violations of copyrights.
Animal welfare
Studies performed on experimental
animals should be carried out according to
internationally recognized guidelines for
animal welfare. That should be clearly
described in the respective section
“Material and methods”.
 Volume 8, Number 3
September 2016

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